Neuritogenesis: The prion protein controls β1 integrin signaling activity

FASEB Journal

Volumn 26, Issue 2, 2012, Pages 678-690

  Loubet, Damien ^a,b   Dakowski, Caroline ^a,b   Pietri, Mathéa ^a,b   Pradines, Elodie ^a,b,f   Bernard, Sophie ^b,c   Callebert, Jacques ^d   Ardila Osorio, Hector ^a,b   Mouillet Richard, Sophie ^a,b   Launay, Jean Marie ^d,e   Kellermann, Odile ^a,b   Schneider, Benoit ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CNRS   (France)

^d HÔPITAL LARIBOISIÈRE   (France)

^e F HOFFMANN LA ROCHE LTD   (Switzerland)

^f ADME T Modeling Platform   (France)

Author keywords

Actin cytoskeleton; Focal adhesions; Neurite sprouting; Neuronal differentiation; Rho kinase

Indexed keywords

ACTIN BINDING PROTEIN; BETA1 INTEGRIN; PRION PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA RHO KINASE; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL POLARITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; NERVOUS SYSTEM DEVELOPMENT; NEURITE; NEUROECTODERM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN STABILITY;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; ANTIGENS, CD29; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; CELL POLARITY; CYTOSKELETON; FIBRONECTINS; LIM KINASES; MICE; NEURAL STEM CELLS; NEURITES; NEUROGENESIS; NEURONS; PRPC PROTEINS; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84856521921     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-185579     Document Type: Article

References (64)

1. Witte, H., and Bradke, F. (2008) The role of the cytoskeleton during neuronal polarization. Curr. Opin. Neurobiol. 18, 479-487
2. Da Silva, J. S., and Dotti, C. G. (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3, 694-704 (Pubitemid 135706675)
3. Witte, H., Neukirchen, D., and Bradke, F. (2008) Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180, 619-632 (Pubitemid 351240708)
4. Gupton, S. L., and Gertler, F. B. (2010) Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Dev. Cell 18, 725-736
5. Geiger, B., Bershadsky, A., Pankov, R., and Yamada, K. M. (2001) Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell. Biol. 2, 793-805
6. Lathia, J. D., Patton, B., Eckley, D. M., Magnus, T., Mughal, M. R., Sasaki, T., Caldwell, M. A., Rao, M. S., Mattson, M. P., and ffrench-Constant, C. (2007) Patterns of laminins and integrins in the embryonic ventricular zone of the CNS. J. Comp. Neurol. 505, 630-643 (Pubitemid 350247130)
7. Tate, M. C., Garcia, A. J., Keselowsky, B. G., Schumm, M. A., Archer, D. R., and LaPlaca, M. C. (2004) Specific beta1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum. Mol. Cell. Neurosci. 27, 22-31 (Pubitemid 39179349)
8. Ma, W., Tavakoli, T., Derby, E., Serebryakova, Y., Rao, M. S., and Mattson, M. P. (2008) Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev. Biol. 8, 90
9. Seidenfaden, R., Krauter, A., and Hildebrandt, H. (2006) The neural cell adhesion molecule NCAM regulates neuritogenesis by multiple mechanisms of interaction. Neurochem. Int. 49, 1-11 (Pubitemid 43669147)
10. Kuwahara, C., Takeuchi, A. M., Nishimura, T., Haraguchi, K., Kubosaki, A., Matsumoto, Y., Saeki, K., Yokoyama, T., Itohara, S., and Onodera, T. (1999) Prions prevent neuronal cell-line death. Nature 400, 225-226 (Pubitemid 29334128)
11. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U. S. A. 95, 13363-13383
12. Kanaani, J., Prusiner, S. B., Diacovo, J., Baekkeskov, S., and Legname, G. (2005) Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J. Neurochem. 95, 1373-1386 (Pubitemid 41779262)
13. Santuccione, A., Sytnyk, V., Leshchyns'ka, I., and Schachner, M. (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J. Cell Biol. 169, 341-354 (Pubitemid 40656571)
14. Graner, E., Mercadante, A. F., Zanata, S. M., Forlenza, O. V., Cabral, A. L., Veiga, S. S., Juliano, M. A., Roesler, R., Walz, R., Minetti, A., Izquierdo, I., Martins, V. R., and Brentani, R. R. (2000) Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res. 76, 85-92 (Pubitemid 30133236)
15. Hajj, G. N., Santos, T. G., Cook, Z. S., and Martins, V. R. (2009) Developmental expression of prion protein and its ligands stressinducible protein 1 and vitronectin. J. Comp. Neurol. 517, 371-384
16. Martins, V. R., Beraldo, F. H., Hajj, G. N., Lopes, M. H., Lee, K. S., Prado, M. M., and Linden, R. (2010) Prion protein: orchestrating neurotrophic activities. Curr. Issues Mol. Biol. 12, 63-86
17. Mouillet-Richard, S., Mutel, V., Loric, S., Tournois, C., Launay, J. M., and Kellermann, O. (2000) Regulation by neurotransmitter receptors of serotonergic or catecholaminergic neuronal cell differentiation. J. Biol. Chem. 275, 9186-9192 (Pubitemid 30185135)
18. Mouillet-Richard, S., Laurendeau, I., Vidaud, M., Kellermann, O., and Laplanche, J. L. (1999) Prion protein and neuronal differentiation: quantitative analysis of prnp gene expression in a murine inducible neuroectodermal progenitor. Microbes Infect. 1, 969-976
19. Lenter, M., Uhlig, H., Hamann, A., Jeno, P., Imhof, B., and Vestweber, D. (1993) A monoclonal antibody against an activation epitope on mouse integrin chain beta 1 blocks adhesion of lymphocytes to the endothelial integrin alpha 6 beta 1. Proc. Natl. Acad. Sci. U. S. A. 90, 9051-9055 (Pubitemid 23306449)
20. Pietri, M., Caprini, A., Mouillet-Richard, S., Pradines, E., Ermonval, M., Grassi, J., Kellermann, O., and Schneider, B. (2006) Overstimulation of PrPC signaling pathways by prion peptide 106-126 causes oxidative injury of bioaminergic neuronal cells. J. Biol. Chem. 281, 28470-28479 (Pubitemid 44414560)
21. Van de Wetering, M., Oving, I., Muncan, V., Pon Fong, M. T., Brantjes, H., van Leenen, D., Holstege, F. C., Brummelkamp, T. R., Agami, R., and Clevers, H. (2003) Specific inhibition of gene expression using a stably integrated, inducible small-interfering-RNA vector. EMBO Rep. 4, 609-615 (Pubitemid 36939953)
22. Robles, E., and Gomez, T. M. (2006) Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat. Neurosci. 9, 1274-1283 (Pubitemid 44454269)
23. Thoumine, O. (2008) Interplay between adhesion turnover and cytoskeleton dynamics in the control of growth cone migration. Cell Adh. Migr. 2, 263-267
24. Naruse, K., Yamada, T., Sai, X. R., Hamaguchi, M., and Sokabe, M. (1998) Pp125FAK is required for stretch-dependent morphological response of endothelial cells. Oncogene 17, 455-463 (Pubitemid 28395910)
25. Panetti, T. S. (2002) Tyrosine phosphorylation of paxillin, FAK, and p130CAS: effects on cell spreading and migration. Front. Biosci. 7, d143-150
26. Zaidel-Bar, R., Ballestrem, C., Kam, Z., and Geiger, B. (2003) Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613 (Pubitemid 37461615)
27. Spector, I., Shochet, N. R., Kashman, Y., and Groweiss, A. (1983) Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219, 493-495 (Pubitemid 13189272)
28. Riento, K., and Ridley, A. J. (2003) Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell. Biol. 4, 446-456 (Pubitemid 36648590)
29. Endo, M., Ohashi, K., Sasaki, Y., Goshima, Y., Niwa, R., Uemura, T., and Mizuno, K. (2003) Control of growth cone motility and morphology by LIM kinase and Slingshot via phosphorylation and dephosphorylation of cofilin. J. Neurosci. 23, 2527-2537 (Pubitemid 36418586)
30. Bernard, O. (2007) Lim kinases, regulators of actin dynamics. Int. J. Biochem. Cell Biol. 39, 1071-1076
31. Pellegrin, S., and Mellor, H. (2007) Actin stress fibres. J. Cell Sci. 120, 3491-3499
32. Legate, K. R., Wickstrom, S. A., and Fassler, R. (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev. 23, 397-418
33. Watts, J. C., Huo, H., Bai, Y., Ehsani, S., Jeon, A. H., Shi, T., Daude, N., Lau, A., Young, R., Xu, L., Carlson, G. A., Williams, D., Westaway, D., and Schmitt-Ulms, G. (2009) Interactome analyses identify ties of PrP and its mammalian paralogs to oligomannosidic N-glycans and endoplasmic reticulum-derived chaperones. PLoS Pathog. 5, e1000608
34. Chen, Z. L., Haegeli, V., Yu, H., and Strickland, S. (2009) Cortical deficiency of laminin gamma1 impairs the AKT/GSK-3beta signaling pathway and leads to defects in neurite outgrowth and neuronal migration. Dev. Biol. 327, 158-168
35. Andressen, C., Adrian, S., Fassler, R., Arnhold, S., and Addicks, K. (2005) The contribution of beta1 integrins to neuronal migration and differentiation depends on extracellular matrix molecules. Eur. J. Cell Biol. 84, 973-982 (Pubitemid 41693201)
36. Hynds, D. L., and Snow, D. M. (2001) Fibronectin and laminin elicit differential behaviors from SH-SY5Y growth cones contacting inhibitory chondroitin sulfate proteoglycans. J. Neurosci. Res. 66, 630-642 (Pubitemid 33032332)
37. Dubash, A. D., Wennerberg, K., Garcia-Mata, R., Menold, M. M., Arthur, W. T., and Burridge, K. (2007) A novel role for Lsc/p115 RhoGEF and LARG in regulating RhoA activity downstream of adhesion to fibronectin. J. Cell Sci. 120, 3989-3998 (Pubitemid 350269404)
38. Huveneers, S., and Danen, E. H. (2009) Adhesion signaling - crosstalk between integrins, Src and Rho. J. Cell Sci. 122, 1059-1069
39. Linden, R., Martins, V. R., Prado, M. A., Cammarota, M., Izquierdo, I., and Brentani, R. R. (2008) Physiology of the prion protein. Physiol. Rev. 88, 673-728 (Pubitemid 351520090)
40. Sakudo, A., Onodera, T., and Ikuta, K. (2007) Prion protein gene-deficient cell lines: powerful tools for prion biology. Microbiol. Immunol. 51, 1-13 (Pubitemid 46155181)
41. Chadi, S., Young, R., Le Guillou, S., Tilly, G., Bitton, F., Martin-Magniette, M. L., Soubigou-Taconnat, L., Balzergue, S., Vilotte, M., Peyre, C., Passet, B., Beringue, V., Renou, J. P., Le Provost, F., Laude, H., and Vilotte, J. L. (2010) Brain transcriptional stability upon prion protein-encoding gene invalidation in zygotic or adult mouse. BMC Genomics 11, 448
42. Shmerling, D., Hegyi, I., Fischer, M., Blattler, T., Brandner, S., Gotz, J., Rulicke, T., Flechsig, E., Cozzio, A., von Mering, C., Hangartner, C., Aguzzi, A., and Weissmann, C. (1998) Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell 93, 203-214 (Pubitemid 28180854)
43. Steele, A. D., Lindquist, S., and Aguzzi, A. (2007) The prion protein knockout mouse: a phenotype under challenge. Prion 1, 83-93
44. Young, R., Passet, B., Vilotte, M., Cribiu, E. P., Beringue, V., Le Provost, F., Laude, H., and Vilotte, J. L. (2009) The prion or the related Shadoo protein is required for early mouse embryogenesis. FEBS Lett. 583, 3296-3300
45. Malaga-Trillo, E., Solis, G. P., Schrock, Y., Geiss, C., Luncz, L., Thomanetz, V., and Stuermer, C. A. (2009) Regulation of embryonic cell adhesion by the prion protein. PLoS Biol. 7, e55
46. Lewis, V., and Hooper, N. M. (2011) The role of lipid rafts in prion protein biology. Front. Biosci. 16, 151-168
47. Mouillet-Richard, S., Ermonval, M., Chebassier, C., Laplanche, J. L., Lehmann, S., Launay, J. M., and Kellermann, O. (2000) Signal transduction through prion protein. Science 289, 1925-1928
48. Pantera, B., Bini, C., Cirri, P., Paoli, P., Camici, G., Manao, G., and Caselli, A. (2009) PrPc activation induces neurite outgrowth and differentiation in PC12 cells: role for caveolin-1 in the signal transduction pathway. J. Neurochem. 110, 194-207
49. Salani, B., Briatore, L., Contini, P., Passalacqua, M., Melloni, E., Paggi, A., Cordera, R., and Maggi, D. (2009) IGF-I induced rapid recruitment of integrin beta1 to lipid rafts is caveolin-1 dependent. Biochem. Biophys. Res. Commun. 380, 489-492
50. Park, J. H., Ryu, J. M., and Han, H. J. (2011) Involvement of caveolin-1 in fibronectin-induced mouse embryonic stem cell proliferation: role of FAK, RhoA, PI3K/Akt, and ERK 1/2 pathways. J. Cell. Physiol. 226, 267-275
51. Bowlus, C. L., McQuillan, J. J., and Dean, D. C. (1991) Characterization of three different elements in the 5′-flanking region of the fibronectin gene which mediate a transcriptional response to cAMP. J. Biol. Chem. 266, 1122-1127 (Pubitemid 21907234)
52. Roman, J., Ritzenthaler, J. D., Bechara, R., Brown, L. A., and Guidot, D. (2005) Ethanol stimulates the expression of fibronectin in lung fibroblasts via kinase-dependent signals that activate CREB. Am. J. Physiol. Lung Cell. Mol. Physiol. 288, L975-L987 (Pubitemid 40547926)
53. Alenghat, F. J., Tytell, J. D., Thodeti, C. K., Derrien, A., and Ingber, D. E. (2009) Mechanical control of cAMP signaling through integrins is mediated by the heterotrimeric Galphas protein. J. Cell. Biochem. 106, 529-538
54. Bito, H., Furuyashiki, T., Ishihara, H., Shibasaki, Y., Ohashi, K., Mizuno, K., Maekawa, M., Ishizaki, T., and Narumiya, S. (2000) A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26, 431-441
55. Kuhn, T. B., Meberg, P. J., Brown, M. D., Bernstein, B. W., Minamide, L. S., Jensen, J. R., Okada, K., Soda, E. A., and Bamburg, J. R. (2000) Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. J. Neurobiol. 44, 126-144
56. Govek, E. E., Newey, S. E., and Van Aelst, L. (2005) The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1-49 (Pubitemid 40095815)
57. Sfakianos, M. K., Eisman, A., Gourley, S. L., Bradley, W. D., Scheetz, A. J., Settleman, J., Taylor, J. R., Greer, C. A., Williamson, A., and Koleske, A. J. (2007) Inhibition of Rho via Arg and p190RhoGAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J. Neurosci. 27, 10982-10992 (Pubitemid 47574156)
58. Threadgill, R., Bobb, K., and Ghosh, A. (1997) Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19, 625-634
59. DeMali, K. A., Wennerberg, K., and Burridge, K. (2003) Integrin signaling to the actin cytoskeleton. Curr. Opin. Cell Biol. 15, 572-582 (Pubitemid 37176966)
60. Clark, E. A., King, W. G., Brugge, J. S., Symons, M., and Hynes, R. O. (1998) Integrin-mediated signals regulated by members of the rho family of GTPases. J. Cell Biol. 142, 573-586 (Pubitemid 28361561)
61. Murakami, H., Iwashita, T., Asai, N., Iwata, Y., Narumiya, S., and Takahashi, M. (1999) Rho-dependent and -independent tyrosine phosphorylation of focal adhesion kinase, paxillin and p130Cas mediated by Ret kinase. Oncogene 18, 1975-1982 (Pubitemid 29150084)
62. Chrzanowska-Wodnicka, M., and Burridge, K. (1996) Rhostimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415 (Pubitemid 26192339)
63. Schoenwaelder, S. M., and Burridge, K. (1999) Bidirectional signaling between the cytoskeleton and integrins. Curr. Opin. Cell Biol. 11, 274-286 (Pubitemid 29164045)
64. Kim, S., and Coulombe, P. A. (2010) Emerging role for the cytoskeleton as an organizer and regulator of translation. Nat. Rev. Mol. Cell. Biol. 11, 75-81